Parasitic fauna of the lake brown trout, Salmo trutta lacustris
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Parasitic fauna of the lake brown trout, Salmo trutta lacustris
Wiadomoœci Parazytologiczne 2009, 55(4), 445–450 Copyright© 2009 Polskie Towarzystwo Parazytologiczne Parasitic fauna of the lake brown trout, Salmo trutta lacustris (Salmonidae), a little known endemic fish from Polish waters Leszek Rolbiecki1, Mariusz Ściążko2, Janusz Schütz3 Department of Invertebrate Zoology, University of Gdańsk, Al. Piłsudskiego 46, 81-378 Gdynia, Poland Wdzydze Manufacturing Fishing Co. Ltd, Czarlina 1, 83-406 Wąglikowice, Poland 3 Regional Department of Environment Protection, Chmielna 54/57, 80-748 Gdańsk, Poland 1 2 Corresponding author: Leszek Rolbiecki; E-mail: [email protected] ABSTRACT. The lake brown trout is a salmonids fish regarded as a stationary form of the migratory trout. Within 2003–2004, 31 lake brown trout (Salmo trutta lacustris L.) from Lake Wdzydze (Poland), were examined for the presence of parasites following commonly used procedures. The parasites found represented Digenea: Diplostomum sp., Posthodiplostomum cuticola (Nordmann, 1832), Sphaerostomum globiporum (Rudolphi, 1802); Cestoda: Eubothrium crassum (Bloch, 1779), Triaenophorus nodulosus (Pallas, 1781); Acanthocephala: Acanthocephalus lucii (Müller, 1776); Copepoda: Ergasilus sieboldi Nordmann, 1832, and Hirudinea: Piscicola geometra (Linnaeus, 1761). The overall infection level amounted to 96.7%, 249.4, and 1–440. The copepod E. sieboldi was the most frequent parasite (93.5%, 257.4, 64–438). Lake brown trout from the Lake Wdzydze are very heavily infected by parasites dominated by the copepod E. sieboldi. Key words: parasites, lake brown trout, Salmo trutta lacustris, Poland Introduction The lake brown trout (Salmo trutta lacustris L.) is a salmonid fish regarded as a stationary, lacustrine form of the migratory sea trout (Salmo trutta trutta L.) or the brown trout (Salmo trutta fario L.). It occurs in lakes of north-western Europe, mainly Scandinavia, Ireland, UK, and Russia, and also in alpine and subalpine lakes. In Poland, native populations of the lacustrine brown trout inhabits catchments of rivers Wda, Brda, and Drawa; in addition, the species, due to stocking operations in the past, this species is present in some water bodies in the southern part of the country and in the Suwałki region. The largest population occurs in Lake Wdzydze (Fig. 1) where it is locally known as the Wdzydze trout. The fish grow to the length of 90 cm and weight 3–10 kg. In case of its occurrence rarity, the lake brown trout is not particularly important commercially, despite of its high quality meat [1,2]. The parasite fauna of the Polish lake brown trout is poorly known. But there are a few papers reporting on studies carried out in 1957–1960 on juveniles (smolts) caught in the Trzebiocha brook discharging into Lake Wdzydze and on adults collected from the Wdzydze [3,4]. In addition, in 1951–1955, Ślusarski [5] studied digeneans in Salmo sp. termed the „Wdzydze trout”; thus it may be assumed that he examined individuals of the lake brown trout. This paper reports on the analysis of the parasitic fauna of the lake brown trout from Lake Wdzydze. The lake is one of the largest in the Pomeranian Lake District. It is located in the Wdzydze Landscape Park, in the river Wda catchment. It is basically a complex of four lakes arranged to resemble an irregular cross, filling the former postglacial troughs and covering a total area of 1455.6 ha; the mean and maximum depths are 15.2 and 68 m, respectively. The Wdzydze receive the discharge of river Wda and its largest tributary, the Trzebiocha, a spawning area of the lake brown trout [6,7]. 446 Materials and methods In March 2003, 26 and 2004, 5 individuals of lake brown trout (25–55 cm, 135–1770 g) caught in Lake Wdzydze were examined (Fig. 1). The fish were dissected to perform a standard parasitological examination. Copepods and leeches (previous narcotised in 50% ethanol), were fixed and preserved in 70% ethanol. The Diplostomum metacercariae (previous killed in hot water) were fixed in 70% ethanol, and 9:1 mixture of glacial acetic acid and formalin was used to fix the remaining helminths; subsequently, all the helminths were preserved in 70% ethanol. Some parasites were mounted whole: copepods whose mouth parts and legs had been dissected out were embedded in lactophenol, while helminths were stained with Gowers carmine, dehydrated in the alcohol series, cleared in benzyl alcohol, and embedded in Canada balsam. Results The study showed total 96.7% of the lake brown trouts have been infected at a mean intensity and intensity range of 249.4 and 1–440, respectively. Altogether 8 parasitic taxa were found. Ergasilus sieboldi represented a dominant species (93.5%, 257.4) (Table 1). Copepods were the only found parasites in fishes captured in 2004. Due to the large morphological similarity between metacercariae representing different species of Diplostomum, identification is very difficult [8]. For this reason, morphometric data [mm] of the two individuals (Fig. 2) collected are reported: body (maximum length and width) first and second specimens, respectively 0.504×0.197, 0.445×0.175; oral sucker 0.047×0.039, 0.055×0.035; length of prepharynx 0.008, 0.004; pharynx 0.031×0.019, 0.031×0.019; acetabulum 0.039×0.043, 0.045×0.043; holdfast organ 0.082×0.070, 0.078× 0.070; distance between acetabulum centre and anterior extremity of body 0.312, 0.292; length of pseudosuckers 0.045, 0.043; width of body at level of pseudosuckers 0.105, 0.074; width of body at level of bifurcation of intestine 0.175, 0.154; width of body at level of mid-length of oral sucker 0.187, 0.166; length of lappet 0.012, 0.012. Excretory bodies (498 and 521) of the two individuals were divided into small (n=30, 0.0095–0.0096×0.0084 –0.0085, mean 0.0095×0.0085) and large groups accounted for 60% of all bodies (n=30, B. Trze bio A. L. Rolbiecki et al. cha Wda W da Lake Wdzydze Fig.1. A. The occurrence of lake brown trout in Poland; B. Lake Wdzydze with large tributaries Explanations: autochthonic populations, location of sampling, introduced populations Parasitic fauna of Salmo trutta lacustris 447 Fig. 2. Diplostomum sp. from lake brown trout from Lake Wdzydze. Scale bar: 0.1 mm 0.0123–0.0124×0.0114–0.0115, mean 0.0123× 0.0114). They were distributed in three elongated fields. Indices: width/length of body (in %): 39; length×width of body/length×width of holdfast organ: 17.3, 14.3; length×width of body/ length×width of acetabulum: 59.2, 40.2; length×width of oral sucker/length×width of acetabulum: 1.1, 1.0; length×width of holdfast organ/length×width of acetabulum: 3.4, 2.8; length ×width of oral sucker/length×width of pharynx: 3.1, 3.3; distance between the centre of acetabulum and anterior extremity of body/length of body (in %): 62, 66; width of body at level of mid-length of oral sucker/width of body at level of bifurcation of intestine: 1.1, 1.1. Discussion The lake brown trout population studied was found to be very heavily infected, primarily by the copepod Ergasilus sieboldi (93.5%, 257.4); the remaining parasites occurred less frequently by prevalence 3.2–12.9% and the mean intensity of 1.0–2.0 parasites per fish. E. sieboldi is common in freshwater fish, and is less frequent in brackish water species (more than 90 species) of numerous families; those preferred include cyprinids, esocids, percids and salmonids [9]. Grabda et. al. [4] who studied fish in the Lake Wdzydze found E. sieboldi to be one of the most common parasite. Out of the 13 fish species examined they recorded this copepod in 8 fish species – common bream Abramis brama (L.), ruffe Gymnocephalus cernuus (L.), vendace Coregonus albula (L.), common whitefish C. lavaretus (L.), northern pike Esox lucius L., roach Rutilus rutilus (L.), S. trutta lacustris, tench Tinca tinca (L.). Lake brown trout was the second (80.0%, 6.5), after tench (88.8%, 50.5), most heavily infected species. Moreover, E. sieboldi was a dominant parasite in lake brown trouts. It is worth 448 L. Rolbiecki et al. Table 1. Parasites of the lake brown trout from Lake Wdzydze Location Prevalence [%] Mean intensity Abundance Range of intensity lens 6.4 1.0 0.06 1 gill filament, palate 6.4 1.0 0.06 1 intestine 12.9 1.0 0.13 1 pyloric caeca 6.4 2.0 0.06 2 liver 3.2 1.0 0.03 1 intestine 3.2 1.0 0.03 1 gill filaments 93.5 257.4 240.8 64-438 gill filaments 12.9 1.0 0.13 1 96.7 249.4 241.3 1-440 Parasites Digenea Diplostomum spp., met. Posthodiplostomum cuticola (Nordmann, 1832), met. Sphaerostomum globiporum (Rudolphi, 1802) Cestoda Eubothrium crassum (Bloch, 1779) Triaenophorus nodulosus (Pallas, 1781), pl. Acanthocephala Acanthocephalus lucii (Müller, 1776) Copepoda Ergasilus sieboldi Nordmann, 1832 Hirudinea Piscicola geometra (Linnaeus, 1761) Total to add that Grabda et al. [4], found this parasite only in lake brown trouts caught during the period of 1957–58. They did not find this parasite in the fishes captured in 1960. The season of catches is quoted as the most likely reason for such situation. Grabda et al. [4], noted in their findings only about seasons (February, March, May, July, October) of catches within the period 1957–58. Moreover, the data do not include the seasonal dynamic of collected parasites. It may be assumed that lack of copepods in 1960 was related to seasonal occurrence of the parasite. The data presented in this manuscript relate to March. Only 13 copepods had egg sacs out of 7465 collected. This study revealed the presence of 8 parasitic species in the lake brown trout. Earlier, Grabda et al. [4] also found 8 parasite species that had infected the Lake Wdzydze fish, 3 parasitic species being present in the fish caught in river Trzebiocha. In addition, Ślusarski [5] recorded 4 fluke species in the trout caught from river Wda. It is worth noticing that the lake brown trout in Europe (including those examined in this study) can be regarded as host for a total of 27 valid parasitic species as well as nonidentified metacercariae of Diplostomum and glochidia [3–5,10] (Table 2). This study provides the second record of the digenean Sphaerostomum globiporum and the copepod E. sieboldi. These two species had been earlier reported only from the lake brown trout inhabiting Lake Wdzydze and river Wda, E. sieboldi being additionally found in river Trzebiocha [3–5]. In spite of previous data that S. globiporum represents a species-specific parasite of roach and rudd Scardinius erythrophthalmus (L.), Grabda et al. [4], concluded that this fluke can be a typical parasite of lake brown trout from Wdzydze Lake. On the other hand, this study provided the first records, in the Lake Wdzydze trout, of Posthodiplostomum cuticola, Eubothrium crassum, Triaenophorus nodulosus, Acanthocephalus lucii, and Piscicola geometra; besides E. crassum and P. geometra were found for the first time in the Lake Wdzydze fish. Moreover, in terms of the entire range of the lake brown trout, P. cuticola, A. lucii, and P. geometra represent first host records. P. cuticola is a parasite mainly of cyprinids and rarely found in other families’ members [11]. A. lucii occurs mostly on predator fishes, including salmonids [12]. Whereas, the hirudinean species P. geometra has very little marked host specificity; in Europe, it has been reported from more than 30 fish species [13,14]. Due to many factors, lake brown trout, as listed above, represents an endemic and rare species. One of these factors are errors in running a lake brown trout school (e.g., excessive farm catches and breaks in fry-stocking) and deterioration of environmental conditions at the spawning ground, which may be the reason of high mortality of fry [6]. It should not be also forgotten about the negative impact of parasites on health state of fishes and in Parasitic fauna of Salmo trutta lacustris 449 Table 2. Variability of lake brown trout parasitic fauna according to various authors Parasites Europe [3–5,10], present Monogenea Gyrodactylus derjavini ? Gyrodactylus truttae Digenea Azygia lucii Bunodera luciopercae Crepidostomum farionis Crepidostomum metoecus Diplostomum spathaceum, met. Diplostomum spp. Posthodiplostomum cuticola Phyllodistomum folium Sphaerostomum globiporum Tylodelphys clavata, met. Cestoda Cyathocephalus truncatus Diphyllobothrium dendriticum, pl. Eubothrium crassum Proteocephalus neglectus (=P. longicollis) Triaenophorus nodulosus, pl. Triaenophorus nodulosus Nematoda Camallanus lacustris Cystidicola farionis Cystidicoloides ephemeridarum (=Sterliadochona tenuissima) Oswaldocruzia filiformis Raphidascaris acus, larv. Acanthocephala Acanthocephalus lucii Neoechinorhynchus rutili Hirudinea Piscicola geometra Branchiura Argulus coregoni Copepoda Ergasilus sieboldi Mollusca Glochidium 1951-55 n=46 [5]* Poland; years of study: 1957-58 and 1960 1957-58 n=35 n=78 [4]** [3]*** Present + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + **** + + + + + + + + + + + + + + + + Explanations: +: parasite reported only from the brown trout from Poland; *: the study focused mostly on juvenile individuals caught in river Wda; **: the study focused on adult individuals caught in Lake Wdzydze; ***: the study focuses on juvenile individuals caught in the Trzebiocha brook; ****: species typical of amphibians and reptilians; according to Moravec [10], it was an accidental infection consequence, on the state of their stock. Grabda et al. [4], drawn also attention to this fact. E. sieboldi seems to be the most dangerous parasite of trout in the Wdzydze Lake. Earlier, prevalence of the parasite infection was 80.0% and the intensity reached 6.5 and 1–17. Infection, at present, increased to 93.5% with high intensity 257.4, 64–438. Such huge infection has an impact on the host. There is no sufficient data related to qualitative and quantitative fauna of parasites composition of lake brown trout school. In earlier studies, it was observed that three species of digeneans and single species within cestodes, nematodes, acanthocephalans, and copepods were present. Currently, 3 species of digeneans, 2 species of cestodes, one species of acanthocephalan, copepod and hirudinea were observed; no nematode was found. It is difficult to make a detailed analysis due to the low prevalence of a majority of parasites and small number of studied fish trials. It could be only established that co- 450 pepod E. sieboldi occurs in huge intensification here, in spite of increased lake eutrofization levels from the 50s, in the 20th century [7]. For comparison, Tuuha et. al. [15], observed the highest parameters of infection in fishes captured from oligotrophic waters, and the lowest in chemically or eutrophically contaminated waters. Probably, aroused differences are related to host specificity. Roach and European perch were studied by Tuuha et al. [15]. As already mentioned, it is difficult to assign the Diplostomum metacercariae to individual species due to high morphological similarity. Metric characters are highly variable within individual species, and often overlap in different species. Most characters of the two individuals studied in this paper differed from Diplostomum spathaceum, previously recorded in trout [3,4]. Thus, it is probable that Diplostomum also represent new host record for the lake brown trout. In summary, it can be concluded that the lake brown trout in Lake Wdzydze is very heavily infected by parasites dominated by the copepod E. sieboldi. References [1] Rolik H., Rembiszewski J. M. 1987. Ryby i krągłouste (Pisces et Cyclostomata). Fauna Słodkowodna Polski, zeszyt 5. PWN, Warszawa. [2] Brylińska M. 2000. Ryby słodkowodne Polski. PWN, Warszawa. [3] Grabda J. 1961. Zdrowotność ryb w potoku Trzebiocha. Roczniki Nauk Rolniczych 93-D: 450-459. [4] Grabda E., Grabda J., Wierzbicki K. 1961. Pasożyty i choroby ryb w jeziorze Wdzydze. Roczniki Nauk Rolniczych 93-D: 239-266. [5] Ślusarski W. 1958. Formy ostateczne Digenea z ryb łososiowatych (Salmonidae) dorzecza Wisły i połu- L. Rolbiecki et al. dniowego Bałtyku. Acta Parasitologica Polonica 6: 247-528. [6] Radtke G. 1997. Problemy badań i ochrony troci jeziorowej Salmo trutta morpha lacustris L. w zlewni jeziora Wdzydze. Przegląd Przyrodniczy 8: 93-96. [7] Lange W., Maślanka W., Nowiński K. 2001. Fizycznolimnologiczne uwarunkowania ochrony jezior. W: Materiały do monografii przyrodniczej regionu gdańskiego, Wdzydzki Park Krajobrazowy, problemy trójochrony (przyroda-kultura-krajobraz). Tom 4. Wydawnictwo Gdańskie, Gdańsk: 55-68. [8] Niewiadomska K. 1996. The genus Diplostomum – taxonomy, morphology and biology. Acta Parasitologica 41: 55-66 [9] Lester R. J. G., Roubal F. R. 1995. Phylum Arthropoda. W: Fish diseases and disorders. Protozoan and metazoan infection. (Ed. P. T. K. Woo). Vol. 1. CABI, Wallingford UK: 475-598. [10] Moravec F. 2004. Metazoan parasites of salmonid fishes of Europe. Academia, Praha. [11] Niewiadomska K. 2003. Pasożyty ryb Polski (klucze do oznaczania). Przywry – Digenea. Polskie Towarzystwo Parazytologiczne, Warszawa. [12] Bauer O. N. 1987. Parazitologičeskie mnogokletočnye. Opredeliteľ parazitov presnowodnych ryb fauny SSSR. Vol. 3. Izdatielstvo Nauka, Leningrad. [13] Elliott J. M., Mann K. H. 1979. A key to the british freshwater leeches with notes on their life cycles and ecology. Freshwater Biological Association. Scientific Publication 40: 1-70. [14] Kearn G. C. 2004. Leeches, lice and lampreys. Springer, The Netherlands. [15] Tuuha H., Valtonen E. T., Taskinen J. 1992. Ergasilid copepods as parasites of perch Perca fluviatilis and roach Rutilus rutilus in Central Finland: seasonality, maturity and environmental influence. Journal of Zoology, London 228: 405-422. Wpłynęło 7 lipca 2009 Zaakceptowano 30 października 2009